Elsevier

NeuroImage

Volume 37, Issue 1, 1 August 2007, Pages 56-70
NeuroImage

Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex

https://doi.org/10.1016/j.neuroimage.2007.05.015Get rights and content

Abstract

Analyzing the brain responses to transcranial magnetic stimulation (TMS) using electroencephalography (EEG) is a promising method for the assessment of functional cortical connectivity and excitability of areas accessible to this stimulation. However, until now it has been difficult to analyze the EEG responses during the several tens of milliseconds immediately following the stimulus due to TMS-induced artifacts. In the present study we show that by combining a specially adapted recording system with software artifact correction it is possible to remove a major part of the artifact and analyze the cortical responses as early as 10 ms after TMS. We used this methodology to examine responses of left and right primary motor cortex (M1) to TMS at different intensities. Based on the artifact-corrected data we propose a model for the cortical activation following M1 stimulation. The model revealed the same basic response sequence for both hemispheres. A large part of the response could be accounted for by two sources: a source close to the stimulation site (peaking ∼ 15 ms after the stimulus) and a midline frontal source ipsilateral to the stimulus (peaking ∼ 25 ms). In addition the model suggests responses in ipsilateral temporo-parietal junction areas (∼ 35 ms) and ipsilateral (∼ 30 ms) and middle (∼ 50 ms) cerebellum. Statistical analysis revealed significant dependence on stimulation intensity for the ipsilateral midline frontal source. The methodology developed in the present study paves the way for the detailed study of early responses to TMS in a wide variety of brain areas.

Section snippets

Experimental procedures

A total of 7 healthy volunteers (2 female, 2 left handed, age 28 ± 3) participated in the study after giving a written informed consent. The study protocol was approved by the Ethics Committee of Helsinki Central University Hospital.

Biphasic magnetic pulses (duration 385 μs) were delivered with a custom-made figure-of-eight coil consisting of two coplanar circular loops (40 mm Ø) so that the induced current was in the posterior–anterior direction. The electromyogram was recorded bilaterally from

Correction of the residual artifact

The data was recorded with an artifact blocking sample-and-hold circuit. Fig. 2A illustrates the dependence of the magnitude of the residual artifacts not blocked by this circuit on stimulus intensity. There was a general trend for increase in artifact magnitude with TMS intensity. However, at the same time the artifact amplitude varied greatly between subjects and in one case high artifact amplitudes were observed even for relatively low TMS intensities. For the specific case of average

Discussion

In the present study we showed that a previously published artifact correction method (Berg and Scherg, 1994) makes it possible to almost completely remove the TMS-induced artifact and reveal physiological EEG responses to TMS, starting as early as 10 ms after the magnetic stimulus. We applied the artifact correction to responses evoked by magnetic stimulation of the left and right M1. Based on the corrected data we suggest a model for the generation of these responses and their dependence on

Acknowledgments

VL was funded by Technion stipend for graduate students, by the German Academic Exchange Service (DAAD) and by Boehringer Ingelheim Fonds. We thank Robert Oostenveld and Eric Maris for their assistance with nonparametric statistical analysis and Naomi Bleich for graphical work.

References (75)

  • Y.Z. Huang et al.

    Theta burst stimulation of the human motor cortex

    Neuron

    (2005)
  • S. Kahkonen et al.

    Distinct differences in cortical reactivity of motor and prefrontal cortices to magnetic stimulation

    Clin. Neurophysiol.

    (2004)
  • S. Kahkonen et al.

    Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans

    NeuroImage

    (2005)
  • S. Komssi et al.

    The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research

    Brain Res. Brain Res. Rev.

    (2006)
  • S. Komssi et al.

    Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation

    Clin. Neurophysiol.

    (2002)
  • C.M. Michel et al.

    EEG source imaging

    Clin. Neurophysiol.

    (2004)
  • Z. Nahas et al.

    Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI

    Biol. Psychiatry

    (2001)
  • A. Pascual-Leone et al.

    Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression

    Lancet

    (1996)
  • R.D. Pascual Marqui et al.

    Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain

    Int. J. Psychophysiol.

    (1994)
  • M. Scherg et al.

    Evoked dipole source potentials of the human auditory cortex

    Electroencephalogr. Clin. Neurophysiol.

    (1986)
  • A. Schnitzler et al.

    Physiological and pathological oscillatory networks in the human motor system

    J. Physiol. (Paris)

    (2006)
  • A. Takashima et al.

    Successful declarative memory formation is associated with ongoing activity during encoding in a distributed neocortical network related to working memory: a magnetoencephalography study

    Neuroscience

    (2006)
  • A. Thielscher et al.

    Linking physics with physiology in TMS: a sphere field model to determine the cortical stimulation site in TMS

    NeuroImage

    (2002)
  • G. Thut et al.

    Effects of single-pulse transcranial magnetic stimulation (TMS) on functional brain activity: a combined event-related TMS and evoked potential study

    Clin. Neurophysiol.

    (2003)
  • G. Thut et al.

    A new device and protocol for combining TMS and online recordings of EEG and evoked potentials

    J. Neurosci. Methods

    (2005)
  • A. Antal et al.

    No correlation between moving phosphene and motor thresholds: a transcranial magnetic stimulation study

    NeuroReport

    (2004)
  • J. Baudewig et al.

    Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS)

    NeuroReport

    (2001)
  • T. Baumer et al.

    Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways

    J. Physiol.

    (2006)
  • S. Bender et al.

    Electroencephalographic response to transcranial magnetic stimulation in children: Evidence for giant inhibitory potentials

    Ann. Neurol.

    (2005)
  • S. Bestmann et al.

    Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits

    Eur. J. Neurosci.

    (2004)
  • D.E. Bohning et al.

    BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS)

    J. Magn. Reson. Imaging

    (2000)
  • G. Cerri et al.

    Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles

    J. Neurophysiol.

    (2003)
  • R. Chen et al.

    Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation

    Neurology

    (1997)
  • A.M. Dale et al.

    Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach

    J. Cogn. Neurosci.

    (1993)
  • Z.J. Daskalakis et al.

    Exploring the connectivity between the cerebellum and motor cortex in humans

    J. Physiol.

    (2004)
  • P. Fox et al.

    Imaging human intra-cerebral connectivity by PET during TMS

    NeuroReport

    (1997)
  • P.T. Fox et al.

    Intensity modulation of TMS-induced cortical excitation: Primary motor cortex

    Hum. Brain Mapp.

    (2005)
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